Download Dynamical patterning modules in plant development and evolution

Int. J. Dev. Biol. 56: 661-674 (2012)
doi: 10.1387/ijdb.120027mb
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Dynamical patterning modules
in plant development and evolution
VALERIA HERNÁNDEZ-HERNÁNDEZ1, KARL J. NIKLAS2, STUART A. NEWMAN3 and MARIANA BENÍTEZ*,1,4,5
Centro de Ciencias de la Complejidad, C3, Universidad Nacional Autónoma de México, Mexico,
2
Department of Plant Biology, Cornell University, Ithaca, NY, USA,
3
Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY, USA and
4
Department of Functional Genomics and Proteomics, CEITEC-Central European Institute of Technology, Brno, Czech Republic,
5
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, México.
1
ABSTRACT Broad comparative studies at the level of developmental processes are necessary to
fully understand the evolution of development and phenotypes. The concept of dynamical patterning modules (DPMs) provides a framework for studying developmental processes in the context
of wide comparative analyses. DPMs are defined as sets of ancient, conserved gene products and
molecular networks, in conjunction with the physical morphogenetic and patterning processes they
mobilize in the context of multicellularity.The theoretical framework based on DPMs originally postulated that each module generates a key morphological motif of the basic animal body plans and
organ forms. Here, we use a previous definition of the plant multicellular body plan and describe
the basic DPMs underlying the main features of plant development. For each DPM, we identify
characteristic molecules and molecular networks, and when possible, the physical processes they
mobilize. We then briefly review the phyletic distribution of these molecules across the various
plant lineages. Although many of the basic plant DPMs are significantly different from those of
animals, the framework established by a DPM perspective on plant development is essential for
comparative analyses aiming to provide a truly mechanistic explanation for organic development
across all plant and animal lineages.
KEY WORDS: dynamical patterning module, plant evo-devo, epigenetics
Introduction
The dynamic characterization of developmental processes is
central to our understanding of the origin and transformation of
form, and thus the evolution of phenotypes (Müller, 2007). Since
multicellularity in plants and animals appears to have independent
origins (Meyerowitz, 2002), studying the dynamics of developmental processes in these two vastly different and diverse kingdoms
enables broad comparative studies to discern both generic and
particular aspects of development (Meyerowitz, 2002).
Newman and Bhat (2008, 2009; see also Newman, 2011) proposed a useful conceptual framework to characterize and compare
basic developmental processes in all multicellular organisms including plants, here broadly defined as all lineages of photosynthetic
eukaryotes, including the various polyphyletic algal clades and
the monophyletic land plant clade, the embryophytes (see Niklas,
2000; Fig. 1). This framework identifies what are called dynamical
patterning modules (DPMs), which are sets of ancient, conserved
gene products and networks in association with ”generic” (i.e.,
common to living and nonliving chemically and mechanically excitable systems; Newman and Comper, 1990) physical effects and
processes they mobilize in the context of the multicellular state.
In animal systems, for example, these physical processes include
cohesion, viscoelasticity, diffusion, spatiotemporal heterogeneity
due to activator-inhibitor interaction, and multistable and oscillatory dynamics (Newman and Bhat, 2008,2009; Newman, 2011).
The DPMs are sufficient to generate the basic features of animal
development (multicellularity, segmentation, pattern formation,
periodic patterning, appendage formation, etc.). By the definition
above, DPMs are inherently associated with the multicellular
Abbreviations used in this paper: DIF, differentiation; DPM, dynamical patterning
module; DTF, developmental transcription factors; FCW, future cell wall; GRN,
gene regulatory network; LLS, leaf-like structure; POL, polarity.
*Address correspondence to: Mariana Benítez. Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México,
Mexico. e-mail: [email protected]
Accepted: 13 August 2012. Final, author-corrected PDF published online: 8 November 2012. Edited by: Mieke Van Lijsebettens.
ISSN: Online 1696-3547, Print 0214-6282
© 2012 UBC Press
Printed in Spain
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V. Hernández-Hernández et al.
state, though they typically originate by the co-option of genes and
regulatory systems already present in the unicellular ancestors of
animals (Newman and Bhat, 2009), fungi and plants (see below).
In addition, DPMs can act alone or in combination, giving rise to a
“pattern language” for the generation of the basic organismic forms
of animals and plants (Newman and Bhat, 2008, 2009).
DPMs are assumed to have been uniquely efficacious in the
origination of multicellular form, as the generic nature of the DPMassociated physical processes makes it plausible that an assortment
of stereotypical forms emerged with relative ease with the rise of
multicellularity (Newman, 1994). In present-day developmental
systems, the body plan- and organ form-generating DPMs may
also continue to operate; however, processes of canalization
(Waddington, 1957), stabilizing selection (Schmalhausen, 1949)
and developmental systems drift (True and Haag, 2001), may have
led to their becoming integrated into more complex pathways.
In conjunction with DPMs, Newman and Bhat (2009) considered
the complementary roles of developmental transcription factors
(DTFs), which are the products of a different subset of ancient
conserved genes from the ones involved in DPMs. The DTFs
and their cognate cis-acting elements comprise gene regulatory
networks (GRNs), which determine cell fate choice and cell differentiation (Davidson and Erwin, 2006), mainly in a cell-autonomous
manner. Together, the DTFs and the DPM-associated molecules
and pathways constitute what Carroll (2001) has called the ”developmental toolkit”. In the case of animals, the gene products
enabling the DPMs are an ”interaction toolkit” (Newman, 2011),
which includes molecules such as cadherins, collagen, Notch,
Wnt, Hedgehog and BMP. In postulating a framework in which the
interplay between DPMs and DTF-associated GRNs provided the
ge
fla
no
di
raw material for the evolution of the metazoans, Newman and Bhat
(2009) also suggested that the evolution of multicellular organisms in other taxonomic groups followed an analogous trajectory
(Newman et al., 2006).
Although the evolutionary history and the origin of multicellularity in plants are not as well-described as in animals, our intention
here is to outline a DPM catalog for plants. We recognize that this
catalog is preliminary and that it will undoubtedly be modified as new
insights into plant development become available. Our goal is to
inform as best as we can future experimental and theoretical work.
Given that plants and animals are different developmentally in
many ways, the nature and role of any DPM operating in plants
likely differ from those described for animals by Newman and Bhat
(Newman and Bhat, 2009; Newman, 2011). In particular, plant
DPMs must incorporate physical limitations on plant development
that differ from those that prevail during animal development.
Despite such differences, we suggest that the concepts of DPMs
and GRNs can help identify a key set of gene products that mobilize
generic physico-chemical processes during plant development.
Moreover, even a preliminary set of plant DPMs could be useful
for comparative studies of plant and animal development that looks
beyond gene homologies, which may not be present or informative, to mechanisms of morphogenesis and pattern formation that
may be shared (or not) at the physical level. Indeed, comparing
gene sequences has provided valuable insights into the evolution of plants, and performing this type of comparison is arguably
easier than comparing more complex entities such as dynamical
patterning modules. However, currently available – and growing
– evidence reveals that a variety of epigenetic factors ranging
from complex regulatory interactions among diverse molecules, to
physico-chemical mechanisms, and organism-environment interactions, are necessary
Arabidopsis
Chara
Funaria
for the generation and variation of plant forms
Chlamydomonas
Coleochaete
Physcomitrella
(e.g., Perry et al., 2007; Peaucelle et al., 2011;
Caulerpa
Cosmarium
Chlorobionta
Polytrichum
Fritschiella
Mesostigma
Niklas and Kutschera, 2012; Uyttewaal et al.,
Spirogyra
Mesotaenium
emb
2012). Hence, in order to fully understand
ryop
hyte
Micrasterias
charo
s
the development of plant phenotypes, and
ytes
phyt
h
p
Netrium
o
r
es
chlo
therefore their evolution, it will be useful to
Penium
extend the current comparative strategies to
Ectocarpus
include those that allow comparing non-linear
pha
Fucus
Rhodophyta
eop
hyte
and multifactorial modules. Defining a basic
s
Stramenopiles
chrys
ophy
Ralfsia
set of plant DPMs is an important starting
tes
point in this challenging undertaking.
cryptophytes
We frame our analysis in terms of the
multicellular plant body plan, as defined by
Alveolates
Niklas and Kutschera (Niklas, 2000; Niklas
and Kutschera, 2009). This body plan is disEuglenoids
tinguished from the unicellular (e.g., Chlamydomonas), colonial (e.g., Phaeocystis), and
siphonous (e.g., Caulerpa) plant body plans
les
Archaea thermophi
by virtue of having symplastic intercellular
s
Bacteria
ile
connections that pass through the walls of
h
p
ido
some or all adjoining cells. The multicellular
ac
body plan has in turn four tissue construction variants: (1) unbranched filaments (e.g.,
Spirogyra), (2) branched filaments that can
Fig. 1. Redacted schematic of the phylogenetic relationships among the two prokaryotic domains be interweaving to give rise to a (3) pseudo(Archaea and Bacteria) and the five major eukaryotic photoautotrophs, collectively referred to as parenchymatous tissue construction (e.g.,
”plants” (euglenoids, dinoflagellates, rhodophytes, chlorobionta and stramenopiles).
Ralfsia), and (4) a parenchymatous tissue
s
te
lla
r ia
ria
te
obac
acte
nob
prote
cya
Dynamical patterning modules in plant evo-devo 663
Cytokinesis and Karyokinesis
Synchronous
Yes
Siphonous
Plane of Cell Division
Indeterminate Growth
1
Unbranched Filaments
2
Branched Filaments
(Pseudoparenchyma)
3
Parenchyma
Yes
Cells Adhere
No
No
Multicellular Colonial Unicellular
No
Yes
Symplastic Continuity
Yes
No
Fig. 2. Developmental features that establish the four plant body plans.
construction, which permits the formation of all other body plan
types (characteristic of all land plants) (e.g., Fritschiella).
Although plants, when broadly defined, constitute a polyphyletic
group (Schlegel, 1994; Graham and Wilcox, 2000; Niklas, 2000),
many of the overall shapes and growth forms observed for plants
are strikingly similar among the different lineages, suggesting an
important degree of convergence. For these and other reasons, the
basic plant body plans, in addition to the common and disparate
molecular components employed during their development, can
be distinguished on the basis of how they achieve their organized
growth (Niklas, 2000). It is in this regard that the DPM concept is
particularly relevant in terms of the key developmental processes
that produce the different plant body plans: (1) the synchronicity
of cytokinesis and karyokinesis, (2) cell-cell adhesion, (3) the establishment of symplastic continuity among adjoining cells, and (4)
the plane of cell division (Niklas, 2000; Fig. 2). Our identification of
plant DPMs further extends and elaborates on these four processes.
In the following sections we will describe basic features of plant
organization and development that in certain aspects set them
apart from the animals. We then present a basic preliminary set of
DPMs, which in recognition of the tremendous diversity observed
across the algal and land plant lineages, is based primarily on
the experimental and developmental information available for the
widely studied annual vascular plant Arabidopsis thaliana. However,
in order to explore the evolutionary origin of these modules, we
track as far as currently possible the presence of certain DPM- and
GRN-associated genes and molecules within and across different
plant lineages. Next, we compare our proposal with other, complementary, attempts to explain the evolution of plant forms, e.g., in
terms of the evolution of certain gene families. Finally, we discuss
the novel aspects of plant DPMs relative to those of animals, and
draw some conclusions about general principles of multicellular
development and its evolution.
Characteristics of plant development and organization
Even though the DPM framework proposed by Newman and
Bhat (Newman and Bhat, 2009; Newman, 2011) is in principle
applicable to all multicellular organisms, plant development has
features that suggest the presence of additional or different sets
of DPMs and perhaps even a different DPM-GRN relationship. In
particular, we note that many plants are characterized by having
open, indeterminate development during which new tissues and
organs are added continuously over the course of their life times.
This mode of development reflects the presence of meristems,
which are composed of pluripotent cells. Among embryophytes,
these stem cells give rise to primary and secondary tissues, as
well as generating new organs.
Another distinguishing feature is that plant growth and development are profoundly influenced by environmental cues and
factors, such as changes in light, nutrient and water availability,
temperature, ecological interactions, etc. The result is a high degree
of developmental plasticity which can produce different morphologies among conspecifics (and even among the same organs of a
single individual). Nevertheless, several developmental features
help to characterize recurrent plant structures that are outcomes
of potentially generic patterning and morphogenetic processes.
In addition to its indeterminate and highly plastic nature, we
note two other fundamental features of plant development. The
first is that plant cells have relatively rigid cell walls such that
morphogenesis must occur in the absence of cell migration to
generate spatiotemporal patterns. Therefore, programmed cell
death and differential asymmetric cell division and growth (e.g.,
De Smet and Beeckman, 2011), as well as the dynamic emergence and regeneration of spatial boundaries and regions take
on particular importance in plant development (Scheres, 2001;
Kim and Zambryski, 2005). In this context, ”spatially dependent
differentiation” refers to the generation of distributions of cell
types associated with heterogeneous patterns of signals. These
patterns are not necessarily instructive chemical fields passively
interpreted by cell arrays (Wolpert, 1996), but may self-organize
during development by complex interactions among genetic and
epigenetic elements (Salazar-Ciudad et al., 2003; Benítez et al.,
2011; Balaskas et al., 2012).
Second, phytohormones such as auxins, cytokinins, ethylene,
abscisic acid, gibberellins, brassinosteroids, jasmonic acid, etc.,
play a central role in the formation of temporal and spatial patterns
during development. Although major aspects of their synthesis,
degradation, transport and cross-regulation have long been
known (see Taiz and Zeiger, 2002), plant hormones and their
signaling systems have only been intensively studied from a
genetic and molecular perspective in recent years. In particular,
the developmental role and the molecular mechanisms associated
with auxin have been extensively characterized (Leyser, 2011;
Wabnik et al., 2011). It is now clear that auxin, in conjunction with
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V. Hernández-Hernández et al.
other phytohormones, participates in the regulation of manifold
developmental transitions and participates in defining regions
that correspond to particular structures and cell types (Niklas
and Kutschera, 2012).
Another key feature of plant development is also closely related
to the non-migrating nature of plant cells and to the dynamics of
spatially dependent differentiation. In the case of animal development, it is relatively easy to distinguish between gene products
and molecules belonging to an interaction toolkit involved in global
DPM-mediated morphogenesis and pattern formation from those
(primarily DTFs) involved in intracellular developmental events,
such as cell-fate determination (Newman and Bhat, 2009). However, in many of the best-studied developmental systems of the
plant model A. thaliana, it is commonly observed that transcription factors involved in cell-fate determination are also involved
in global patterning processes, e.g., flower organ determination
(Urbanus et al., 2010), epidermal cell patterning (Kurata et al.,
2005) and meristem subspecification in the root (Cui et al., 2007).
Indeed, it has been shown that the mobilization of transcription
factors and other molecules through plasmodesmata (channels
traversing cell walls and enabling transport and communication
between cells), plays a central role during plant developmental
processes (Kim and Zambryski, 2005). Although intercellular
transport of developmental transcription factors is not unknown
in animal systems, it is extremely rare (Prochiantz, 2011).
In addition to being a continuum relative to the action of developmental transcription factors, plant tissues are permissive to the
direct cell-cell transport of soluble signaling factors such as auxins
and other phytohormones. In contrast to animal morphogens, these
molecules can act intracellularly as transcriptional modulators
and determinants of the differentiated state (see, for example,
Garrett et al., 2012). Nevertheless, unlike animal morphogens,
phytohormones exert a more direct transcriptional regulation and
have a strong morphological impact during the whole life cycle of
the organism. The direct transcriptional roles of morphogens, like
the aforementioned cell-to-cell transport of transcription factors,
blur the functional separation of GRNs (single-cell determinants
of cell differentiation) and DPMs (multicell determinants of pattern formation and morphogenesis) seen in animal development
(Newman and Bhat, 2008, 2009).
Basic dynamical patterning modules (DPMs) in plants
Herein, we present each of the postulated DPMs in the context
of what we consider key developmental events and processes
in plants. We also discuss the possible origin of these modules
in the light of the presence of the characteristic molecules they
deploy in different plant lineages. Some of these modules have
been studied by other authors (e.g., Green, 1962; Lindenmayer,
1975; Sachs, 1991), and have been postulated as important
mechanisms in plant development and evolution. In this contribution, we present these mechanisms in the context of recent
experimental evidence and integrate them within the theoretical
framework of dynamical patterning modules.
Future cell wall (FCW)
A critical developmental module in plant evolution is a system
that defines the orientation and location of the cell wall during cell
division, which in turn results in the formation of different types
of tissue construction (Niklas, 2000). Among the charophycean
algae and the embryophytes, the location of the future cell wall is
prefigured by the appearance of the preprophase band and the
phragmoplast (Brown and Lemmon, 2011). The mechanisms underlying the orientation and location of these cytological features
are under investigation but not well understood (see for example
Gibson and Gibson, 2012). However, early in the 20th century,
workers reported that the application of pressure to a dividing cell
forced the mitotic figure into the position in which the longitudinal
axis was oriented at right angles to the applied pressure such that
the future cell wall was oriented parallel to this direction (Kny, 1902;
see also Lynch and Lintilhac, 1997). Likewise, Steward and coworkers (1958) noted that cells in free suspension have highly irregular
and unpredictable planes of division, perhaps because they are not
restricted peripherally as they would when cells normally grow within
the plant body. Among certain colonial cyanobacteria, flagellates,
and pollen sporocyctes wherein cell divisions are simultaneous,
the planes of successive division tend to be at right angles to one
another such that regular patterns of two, four, eight, etc. form,
all in one plane (Geitler, 1951). A complementary geometric view
of this process is known as Errera’s rule and has recently been
explored as a modeling approach (Besson and Dumais, 2011).
That biomechanically induced mechanical stresses may be involved in cell wall orientation is consistent with many observations
(e.g., Corson et al., 2009, although see Mirabet et al., 2011). The
simplest plant cells are parenchyma cells, which have thin primary
walls and are therefore hydrostatic. The turgor pressure exerted
against the walls of these cells is more or less uniform. However,
at the vertices created by adjoining cells, opposing tensile stresses
are resolved into additional stresses acting in the radial direction
on the angle of each vertex according to its size. In theory, the
tensile stresses in walls at 180º should be equal and opposite and
thus this angle experiences no additional radial stress from the
resolution of the opposing tensile stresses in the two intersecting
walls. However, these tensile stresses are resolved into progressively larger radial stresses as the angle of a vertex decreases,
reaching their maxima as the angle approaches 0º. Because
these additional radial stresses are correlated directly to the size
of the angle, a cell reaches mechanical equilibrium at equiangular
vertices. Consequently, the observation that the vertices in the
region of isodiametrical expansion can act as cellular pivots for
wall rotation between successive divisions (so as to coincide with
cellular mechanical equilibria) provides some evidence for the
biomechanical regulation of cell shape (Niklas and Spatz, 2012).
This biomechanical scenario is vastly different from that operating in an elongating cell (e.g., xylem fiber), wherein existing
walls rotate around their vertices to align either perpendicular or
parallel to the longitudinal axis and future cell walls are generally
oriented perpendicular to the growth axis. Here, the principal
stress trajectories likely resolve the global stress patterns into
orthogonal components and are thus likely to be oriented parallel
and perpendicular to the growth axis. In this condition, cell walls
may be oriented so as to minimize shear stresses.
Neither of these scenarios addresses the issue of whether cell
walls directly transduce radial stresses into specific cell shapes,
or whether mechano-sensitive elements in the cell membrane or
cytoskeleton take on or augment this function. However, it is reasonable to suppose that a ”future cell wall” (FCW) module exists,
that it is ancient, and that it involves physical cues resulting from
Dynamical patterning modules in plant evo-devo 665
mechanical stresses operating in preexisting cell walls resulting
from hydrostatic pressures (Table 1; Fig. 3).
The effects on multicellular organization of intracellular patterning processes in a founder cell such as an egg or stem cell
have been discussed for animal systems under the rubric of ”autonomous” patterning mechanisms (Salazar-Ciudad et al., 2003).
Because DPMs only come into play in animal embryos when a
critical number of cells have been generated (e.g., at the morula or
blastula stage), it has been suggested that disparate autonomous
patterning processes that may occur in the eggs of subphylum taxa
serve mainly to set the initial and boundary conditions for DPM
implementation, with conservation of DPM-determined ”phylotypic”
body plans (Newman, 2011). However, because of the immobility
of plant cells, an autonomous patterning mechanism like FCW
would be expected to have more profound consequences for plant
body plan organization, placing it more in the DPM category. The
biological differences between plants and animals are thus manifest
even at this most basic level.
Cell-cell adhesion (ADH)
One of the requisites for multicellularity is the presence of
mechanisms and molecules that enable cell-cell adhesion (ADH),
which is achieved in different ways in plants, animals and fungi
(Knox, 1992; Abedin and King, 2010; Wolf et al., 2012). Among the
land plants, cells remain together mainly due to the presence of
pectin polysaccharides in the middle lamella associated with the
primary cell walls of adjoining cells, which constitute the so-called
pectic matrix in which other structural cell-wall components, such
as cellulose, hemicellulose and lignin are embedded (Knox, 1992;
Willats et al., 2001; Jarvis et al., 2003) (Fig. 3).
The cell wall constitutes one of the characteristic features of
plant cells and, arguably, its presence has significantly affected the
evolution of plant development. As noted, the cell wall restricts cell
mobility, precluding a role for cell migration in plant development.
Indeed, the cell wall begins to be formed from cell plates during
cytokinesis, such that cell adhesion is the default state (Knox, 1992;
Jarvis et al., 2003), which confers mechanical strength by virtue
of an ”endoskeleton” in the multicellular plant body plan (Niklas,
1992). Additionally, the proportion and chemical state (e.g., level of
esterification) of each of the cell wall components is spatiotemporally regulated over the course of development, locally as well as
globally, adjusting the mechanical properties of cells and tissues,
and contributing to the regulation of cell and organ growth, as well
as to organogenesis (Jarvis et al., 2003; Peaucelle et al., 2011).
Moreover, diverse mechanisms for pattern formation have evolved
in the presence of the plant cell wall.
The original proposal of dynamical patterning modules maintains
that modules typically have their origin in the co-option of genes
and regulatory systems already present in the unicellular ances-
tors of animals, and potentially plants and fungi (Newman and
Bhat, 2009). The evolution of cell adhesion can then be studied in
plants by exploring the evolution of the cell wall, and particularly,
by investigating the presence of pectin polysaccharides and other
components of the wall in different plant lineages, including the
algae, as well as in groups of unicellular organisms that are closely
related to plants. For example, embryophytes and charophycean
algae share a common unicellular ancestor that undoubtedly had
cell walls (Graham, 1996; Niklas and Kutschera, 2012). However,
the question of whether the unicellular ancestors of land plants
had the cell-wall molecules that enable cell-cell adhesion remains
open, as the composition of the cell wall considerably differs among
extant orders of the charophycean algae (Sørensen et al., 2011).
Some cell wall components have ancient origins while others
have emerged with specific plant taxa or plant tissues (Sørensen
et al., 2011). Primary cell walls are mainly conformed by cellulose
microfibrils bound together by cross-linking hemicelluloses that
include xyloglucans (XyG), xylans, arabinoxylans, mannans and
mixed-linkage (1→3), (1→4)-b-D-glucan (MLG). In turn, the primary cell wall is embedded in a matrix of pectin polysaccharides
that include homogalacturonan (HG), rhamnogalacturonan I (RGI)
and ramnogalacturonan II (RGII), as well as some proteins and
proteoglycans (Ridley et al., 2001). The secondary wall of vascular
plants contains more hemicelluloses than pectins and is reinforced
by the phenylpropanoid polymer lignin (Boerjan et al., 2003).
The cellulose synthase genes (CesA) are widespread among
eukaryotes and prokaryotes (Popper et al., 2011). Remarkable
molecular homologies exist among the functionally non-redundant
CesA genes across diverse clades, and the presence of these genes
in diverse lineages (including animals) may be the result of lateral
gene transfers during the origins of eukaryotic lineages (Niklas,
2004). Ultrastructural comparisons of the trans-membrane complexes containing CesA proteins support this hypothesis (Delmer,
1999; Richmond and Somerville, 2000; Nobles et al., 2001; Roberts
et al., 2002). All members of the CesA gene family isolated from
embryophytes encode for integral membrane proteins with one
or two transmembrane helices in the N-terminal protein region,
three to six transmembrane helices in the C-terminal region, and
an N-terminal domain structure that includes a cytoplasmic loop
of four conserved regions (U1–U4), each of which contains a D
residue or the QXXRW sequence, which is predicted to code for
glycosyltransferase functionality (Richmond and Somerville, 2000).
Three additional shared features are a CR-P region between the
U1 and U2 conserved regions, an N-terminal LIM-like zinc-binding
domain, and a region between U2 and U3 (Delmer, 1999) that is
conserved within specific clades (Vergara and Carpita, 2001).
Molecular comparisons indicate that the CR-P insertion and
the D-D-D-QXXRW motif evolved before the appearance of the
embryophytes – indeed, before that of eukaryotes – because both
TABLE 1
PLANT DYNAMICAL PATTERNING MODULES (DPMs)
DPM
Characteristic molecules
Physical processes
Evo-devo role
FCW
Cell wall components, possible mechanosensitive elements
Mechanical stress
Defines the orientation and location of the cell wall
ADH
Cell wall components, mainly pectin polysaccharides
Adhesion
Formation of multicellular organisms
DIF
Plasmodesmata components
Diffusion, reaction-diffusion-like mechanisms
Pattern formation and cell type specification
POL
Auxin, auxin polar transporters, and cell wall components
Mechanical stress
Polarity, axis formation and elongation
BUD
Auxins, auxin polar transporters, expansins, and cell wall components
Lateral inhibition and buckling, deformation
Periodic formation of buds and lateral roots
LLS
Cell wall components
Buckling, compression-expansion
Formation and shaping of leaf-like structures
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V. Hernández-Hernández et al.
features have been identified in CesA proteins from the green alga
Mesotaenium caldariorum (Roberts et al., 2002) and in CesA-like
proteins from cyanobacteria (Nobles et al., 2001). Thus, the genome
for cellulose biosynthesis may be traceable to the endosymbiotic
origins of chloroplasts, a key event in the history of life. Subsequent
gene duplication and functional divergence occurred after ancient
CesA-like genes were integrated within eukaryote genomes, because eukaryotic CesA proteins are functionally non-redundant and
are arranged in structurally well defined transmembrane structures,
called terminal complexes, which are invariably involved in cellulose
assembly and deposition into the cell walls of the Phaeophyta,
Chrysophyta, Chlorophyta, and Embryophyta (Kutschera, 2008).
Among other cell wall components, XyG epitopes have been
found in Netrium digitus, Chara coralina, Coleochaete nitellarum
and Cosmarium turpiniand and to a lesser extent in Spirogyra sp.
(Sørensen et al., 2011). A XyG endotransglucosylase activity and
a putative XyG endotransglucosylase/hydrolase enzyme were
detected in Chara vulgaris (Van Sandt et al., 2007). RGII has not
been found in charophycean green algae, but it is possible that they
are capable of synthesizing the backbone of RG. Two rare 2-keto
sugars 2-keto-3deoxyoctonate (KDO) and 3-deoxy-2heptulosaric
acid (DHA) that are present in RGII also occur in the elaborate
scales of some prasinophyte algae (Becker et al., 1998) and DHA
occurs in Mesostigma viride (Domozych et al., 1991). This indicates
Fig. 3. Schematic representation of the six dynamical patterning modules. (see Table 1). Abbreviations: CW, cell wall; Cyto., cytoplasm; FCW,
future cell wall; Leaf. Pr., leaf primordium; Plasmo., plasmodesmata; Pol.
Trans., transmembrane polar transporter; SAM, shoot apical meristem.
the early evolution of an RGII-like core structure and its posterior
diversification during the evolution of embryophytes (Sørensen
et al., 2011).
Xylans seem to be present in vascular plants, hornworts and
red algae (Popper et al., 2011; Sørensen et al., 2011). Also, Ostreococcus, the smallest known eukaryote and a member of the
charophycean green algae, contains several glycosyl transferases
that differ from those found in land plants, but which might have
a role in xylan biosynthesis (Popper et al., 2011). Other cell wall
components that could have been an inheritance from algal ancestor are mannans, HG and arabinogalactans (Sørensen et al.,
2011). HG has been detected in the walls of the unicellular desmid
Penium margaritaceum and in the charalean species C. coralina
(Sørensen et al., 2011). This supports the hypothesis that many
cell wall features of land plants evolved prior to terrestrialization
(Sørensen et al., 2011; Popper et al., 2011).
Overall, these studies suggest that plant unicellular ancestors
had at least some of the cell-wall components that underlie cell-cell
adhesion and that these were co-opted in the transition to multicellularity. The production of an external envelope of mucoids, or of a
composite of calcium pectate and hemicelluloses, is widespread in
the cyanobacteria and in the brown, red, and green algal lineages. In
addition to protecting cells from herbivores, these materials function
as an attachment mechanism to substrata and in the fertilization
of water suspended gametes (Graham and Wilcox, 2000). That
these components could have been recruited to the organization
of multicellular tissues can be inferred from the behavior of an
analogous fungal system: certain genotypes of the generally unicellular yeast Saccharomyces cerevisiae can aggregate (Smukalla et
al., 2008) or remain attached postmitotically (Ratcliff et al., 2012)
under various genetic or environmental conditions.
Spatially dependent differentiation (DIF)
Embryophytes, and many algal lineages with a multicellular body
plan (sensu Niklas, 2000), exhibit cell differentiation. Indeed, most
of them have meristematic regions, either apical or intercalary,
in which proliferation and differentiation zones are maintained in
a steady, yet dynamic balance. An important mechanism for the
maintenance of zones with a particular cell identity is the inheritance
of a cellular fate through cell lineages (Scheres, 2001). This is especially evident in the root of A. thaliana, where cells of a particular
type are arranged in lines of cells belonging to the same lineage
(Scheres, 2001). However, the de novo specification of cellular
identities and regions within the plant body seems to rely mostly
on asymmetric cell division (De Smet and Beeckman, 2011) and
on the generation of spatiotemporal patterns that distinguish a cell
or a region from its neighbors (Scheres, 2001).
For this DPM, we focus on the spatially dependent differentiation
and patterns that underlie key events in cell-fate determination and
organogenesis. We term this the spatially dependent differentiation (DIF) DPM (Table 1; Fig. 3). In contrast to animal embryos in
which cell differentiation is mediated mainly by intracellular GRNs
(not DPMs), and pattern formation controlled by several distinct
DPMs involving cell rearrangement (Newman and Bhat, 2008,
2009), plant cells walls preclude local rearrangement. Significantly,
however, such walls have channels that allow symplastic movement of molecules between cells (Kim and Zambryski, 2005). In
this manner, rather than cells, molecules such as transcription
factors, peptides, RNA, auxins and other morphogens, migrate or
Dynamical patterning modules in plant evo-devo 667
translocate during plant development. Symplastic communication
relying on the presence of these channels (plasmodesmata) (Raven
et al., 2005) has been identified by Niklas (2000) as a diagnostic
characteristic of the multicellular plant body plan. By enabling
fluxes of molecules across cell boundaries, plasmodesmata interconnect intracellular regulatory networks and play a central role
in the formation of spatiotemporal patterns of gene expression at
the whole organism level (Kim and Zambryski, 2005; Lucas et al.,
2009; Lehesranta et al., 2010).
Although membrane transporters are not involved, the plasmodesmata-mediated movement of molecules appears to be tightly
regulated and to depend on the type and size of the mobile molecule,
as well as on the particular tissue, and developmental stage (Kim
and Zambryski, 2005). Although the details of this type of regulation
are only starting to be uncovered, an important aspect of spatially
dependent differentiation through cell-cell communication is that
it constitutes a dynamic process in which differentiating cells and
developing tissues play an active role in setting up the signaling
system that pattern them – in contrast to the dissociation between
these roles suggested by cells ”reading” or ”interpreting” positional
information (Wolpert, 1996). As noted, unlike animal development,
transcription factors and the GRNs in which they participate may
act transcellularly during plant development, whereas globally
transported morphogens can act at the transcriptional level (e.g.,
Garrett et al., 2012). Insofar as this is true, cell fate determination
and multicellular patterning are inseparable, justifying the designation of a plant-specific spatially dependent differentiation DPM.
Some of the best-studied plant developmental systems involve
the movement of molecules through plasmodesmata (see reviews
in Kim and Zambryski, 2005; Benítez et al., 2011; Tusscher and
Scheres, 2011). For example, symplastic cell-to-cell communication
is necessary for the establishment and maintenance of meristems,
which are fundamental for the continuous growth and patterning of
multicellular plants. In the root apical meristem and in the vascular
meristem of A. thaliana the establishment of the regions harboring
pluripotential cells, as well as the regulation of proliferation and
differentiation in these regions during post-embryonic development,
require the cell-to-cell movement of transcription factors or other
regulatory molecules through plasmodesmata (e.g., Tusscher and
Scheres, 2011; Perilli et al., 2012).
In principle, the presence of symplastic channels can mobilize
physical processes that have been shown to contribute to pattern
formation and that are thus part of the DIF DPM (Table 1). The
most obvious of these processes is simple passive diffusion. In
turn, intercellular concentration gradients generated by diffusion
can contribute to the regulation of gene expression, the cell cycle,
and other intracellular processes. Moreover, it has been proposed
that in some plant developmental systems, plasmodesmata enable
a type of generic physico-chemical patterning mechanism known
as reaction-diffusion (Pesch and Hülskamp, 2004; Jönsson et al.,
2005; Benítez et al., 2011), which also includes lateral inhibition
mechanisms (see below).
Reaction-diffusion systems (RD), as originally proposed by
Turing (1952), consist of two or more chemicals that react with
each other and that are able to diffuse. Depending on its diffusion
and reaction rates, the chemical system can produce complex
concentration patterns, ranging from spaced-out dots to fringes and
labyrinths. Examples in plant development exist in which complex
patterns of cell types seem to emerge, at least in part, from RD-like
mechanisms (Benítez et al., 2011). However, as is the case with
the utilization of this mechanism in animal patterning (Kondo and
Miura, 2010; Zhu et al., 2010), in these systems, there seems to
be sets of genes and gene products, and tissue-scale transport
processes in addition to diffusion collectively behaving like a RD
system, rather than a simple pair of reacting and diffusing chemicals. Indeed, regulatory processes underlying pattern formation
in plants may be dynamically richer than RD systems, e.g., they
may exhibit redundancy at the gene or at the ”circuit” level in ways
that confer the patterning systems with dynamic properties that are
atypical of simple RD systems (Benítez et al., 2011).
Plasmodesmata are present in embryophytes and the charophycean algae (collectively called the streptophytes), since
current evidence suggests that these intercellular connections
are homologous (Graham et al., 2000). This homology, however,
does not address the origins of these symplastic connections in
terms of the last common unicellular ancestor of this large lineage.
The origin of plasmodesmata and plasmodesmata-like structures
among the various plant lineages may be the result of lateral
gene transfer during primary or secondary endosymbiotic events
(Niklas, 2000). Multicellularity has evolved in some cyanobacteria
(photosynthetic bacteria), which possess small channels that cross
walls of neighboring cells. Since chloroplasts likely evolved from a
symbiotic event with cyanobacteria, it is possible that part of the
genetic toolkit for constructing symplastic conduits in the various
algal lineages trace their evolutionary origins to the cyanobacteria.
Whether or not this is the case, it will be important to study the
evolution of particular molecules involved not only in plasmodesmata
structure, but also those involved in the regulation of molecular
trafficking through plasmodesmata (Lucas et al., 2009).
Polarity and the determination of the apical-basal axis (POL)
Among multicellular plants, the polarization of the body axis
relies to a great extent on cell-level polarization processes. These
can change in response to internal and external cues, making the
establishment and maintenance of cell polarity, and concomitant
organ polarity, a plastic process during plant development. Here,
we describe the POL dynamical patterning module that appears
to underlie short and long-range polarization, as well as the
specification of an apical-basal growth axis. This DPM involves
the phytohormone auxin and the mechanical forces generated in
the plant cell-wall (Table 1; Fig. 3).
Auxin is involved in a large spectrum of developmental processes,
including cell expansion and differentiation (Taiz and Zeiger, 2002;
Niklas and Kutschera, 2012). Among the vascular plants, auxin is
synthesized in shoot and root apical meristems from which it can
be transported symplastically or through extracellular spaces (apoplastic transport). In the former case, the family of PIN-FORMED
(PIN) auxin efflux carriers is largely responsible for the formation of
auxin gradients, as the localization of these transporters in particular regions of the cell membrane creates and directs auxin fluxes.
Moreover, PINs can be continually rearranged and re-targeted to
different regions of the cell membrane. The positioning of PINs
provides a mechanism that establishes the directionality of auxin
fluxes, whereas the repositioning of PINs provides a mechanism
to change the polarity of cell, tissue, or organ growth. Importantly,
polarity can be defined at the cell level and at the organ level and
while they are tightly linked, the two do not necessarily coincide
(e.g., in the shoot apex PIN1 polarity is well-defined while there
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V. Hernández-Hernández et al.
is no overall polarity in the central and peripheral zone). The detailed mechanisms responsible for establishing, maintaining, and
changing PIN arrangement are just beginning to be uncovered. It
appears, however, that they may involve the regulation of trafficking of intracellular vesicles, the regulation of cytoskeleton alignment, or other signaling events (for a recent review, see Niklas
and Kutchera, 2012).
The plant cell wall is another important factor in determining
cell polarity because the rate and direction of cell growth involves
the disposition and arrangement of the cell wall components
(Cosgrove, 2005), and it occurs in the direction dictated by a set
of physical forces. From a mechanical perspective, the mature
cell wall is a rigid composite that exerts a hydrostatic compressive
force when the protoplast it surrounds is turgid. Any permanent
increase in the volume of the protoplast (i.e., growth) requires the
loosening of the cell wall, which permits the influx of water and
an increase in cell volume (Cosgrove, 2005). Cell wall loosening
allows for wall stress relaxation (i.e., a reduction in cell wall mechanical stresses) (Niklas, 1992; Cosgrove, 2005; Mirabet et al.,
2011). Consequently, when the cell wall is relaxed, turgor pressure
provides the mechanical energy that is required to expand the cell
(Cosgrove, 2005; Boudaoud, 2010; Mirabet et al., 2011). However,
the direction of cell growth depends on the extent to which cell
wall constituents (primarily, cellulose microfibrils) are uniformly
or asymmetrically distributed in the cell wall. If stress-resisting
constituents are homogeneously distributed, cell expansion is
more or less uniform (isotropic growth). If these constituents are
heterogeneously distributed, cell expansion is anisotropic. Polar
cell growth, therefore, requires a prefigured deposition of cell wall
stress-resisting constituents (Niklas and Spatz, 2012).
Experimental evidence in A. thaliana and other plant models
indicates that auxin flow and cell-wall forces reciprocally interact
during the emergence of polarity. Auxin promotes polar expansion
through cell wall loosening, probably by means of the acidification
of the apoplast and the concomitant disruption of non-covalent
bonds among cell wall polysaccharides (Cosgrove, 2005). In turn,
the preferential localization of PINs (or their transporting vesicles),
which determines auxin fluxes, may target where cell wall loosening occurs (Heisler et al., 2010).
We propose that auxin mobilization and the effects of auxin
on the mechanical properties of the cell wall provide a DPM that
establishes the polarity of the body axis throughout the multicellular plants. It is likely that elements of this module were present
in unicellular plants since the cell walls of unicellular algae are
not mechanically isotropic and manifest morphologies that are
distinctly non-spherical. In addition, endogenous auxin has been
identified in some multicellular algae (Boot et al., 2012), even in
lineages that are not related to the green algal and land plant clade
(e.g., the brown alga Ectocarpus siliculosus, in which auxin might
play a crucial role in the elongation of the filamentous thallus; Le
Bail et al., 2010). Likewise, the effects of auxins on the dynamics
of the cytoskeleton of unicellular charophycean algae appear to
be similar to those observed for embryophytes (Jin et al., 2008).
Innovations in auxin biosynthesis and metabolism have led to
more precise regulation of auxin levels (Cooke et al., 2002; Křeček
et al., 2009) and the origination and diversification of the auxin
transporters (e.g., plasma membrane PINs) have contributed to the
diversification of land plant body plans (Zažímalová et al., 2010).
However, although Fujita and collaborators (2008) detected auxin
fluxes in the sporophyte of three species of mosses, Physcomitrella patens, Funaria hygrometrica and Polytrichum commune,
they found no evidence for auxin fluxes in gametophytic “shoots”
nor did they find any putative orthologs of plasma membrane PIN
transporters. Additionally, De Smet and coworkers (2011) concluded that mosses do not posses plasma membrane PINs but
may have putative orthologs for PINs localized in the membrane
of the endoplasmic reticulum. These and other lines of evidence
indicate that some type of anisotropic auxin mobilization (sensu
Wabnik et al., 2011) or some other, still-unknown transporters may
be involved in the formation of auxin fluxes in algae and mosses
(e.g., Boot et al., 2012). If true, the potentially generic POL module
may have evolved from some form of anisotropic auxin mobilization that did not necessarily involve plasma membrane PINs but
instead involved cell wall mechanical stresses.
That the POL DPM may draw on ancient physiological properties of the plant cell can be inferred from the studies of Jaffe and
coworkers on rhizoid formation during the embryogenesis of the
brown alga, Fucus (Jaffe, 1969; Peng and Jaffe, 1976). All eukaryotic cells are capable of generating intracellular spatiotemporal
transients in calcium ion concentration. In Fucus, the position of
the rhizoid, a morphological protuberance of the cell that is the
first sign of developmental polarity, is not predetermined, but is
induced in the fertilized egg by an asymmetric calcium flux from
the cell elicited by a light gradient or any of a number of different biochemical manipulations which mobilize and organize this
generic unicellular functionality (see also discussion in Smith and
Grierson, 1982).
Periodic formation of buds (BUD)
As noted, auxin participates in the DIF and POL dynamical patterning modules. Here, we propose a third module in which auxin
plays a significant role, but in which the key physical process is
lateral inhibition. This is the periodic formation of buds and lateral
roots (BUD) DPM (Table 1; Fig. 3).
After germination, the typical vascular land plant continues to
grow and develop new roots, stems, and leaves. New roots are
added as a result of the endogenous development of new root
apical meristems. In contrast, new stems and leaves are the result
of the exogenous development of leaf primordia, which develop
into a variety of leaf-types (e.g., bracts, foliage leaves, and petals)
and axillary buds, which can develop into new shoots. The shoot
apical meristem produces leaf primordia in a highly regulated
process that gives rise to different arrangements of leaves, e.g.,
different phyllotactic patterns (Douady and Couder, 1996; Reinhardt, 2005; Besnard et al., 2011). The stereotypical phyllotactic
patterns (alternate, opposite, whorled or spiral), which are found
in almost all vascular land plants (Reinhardt, 2005), can change
during plant development. For example, many plants transit from
an initial decussate phyllotaxis to a spiral pattern, during reproductive development, and finally to whorled phyllotaxis during
floral development (Reinhardt, 2005). These transitions suggest
the existence of a potentially common organogenic mechanism
behind all phyllotactic patterns (Reinhardt, 2005; Jönsson et al.,
2005; Newell et al., 2008) that can be studied, at least partially,
by investigating the mechanisms that specify the positions of leaf
primordia (Jönsson et al., 2005; Besnard et al., 2011).
Several experiments indicate that preexisting primordia influence the location of new ones (Reinhard, 2005; Bohn-Courseau,
Dynamical patterning modules in plant evo-devo 669
2010). This phenomenology was the basis for the hypothesis that
the formation of new primordia is mediated by the diffusion of an
inhibitory molecule that blocks the emergence of primordia next
to each other (see review in Reinhardt, 2005). According to this
hypothesis, each primordium is an auxin sink and the distance
between newly formed primordia depends on the concentration
of a negative regulator that peaks in the position of an emerging
primordium and decreases with increasing distance from this site.
At some threshold level, the inhibitor ceases to prevent the formation of other primordia.
In the general case, this hypothesis invokes a lateral inhibition mechanism that, theoretically, suffices to generate observed
phyllotactic patterns rigorously conforming to the mathematical
Fibonacci series. As Douady and Couder (1996) showed theoretically, and experimentally, using a nonliving system of sequentially
deposited magnetic droplets, a generic self-organizing process
depending on the successive appearance of new elements that
are repelled from each other gives rise to periodic patterns similar to the phyllotactic ones. Moreover, this mechanism provides
a physical system in which comparatively small changes in one
or few parameters give rise to transitions in phyllotactic patterns
(Douady and Couder, 1996).
The processes that underlie this kind of a lateral inhibition
mechanism in living plants remain unknown. Recently, however, the
development of molecular-genetic tools has provided the means to
test whether such a mechanism exists in model organisms like A.
thaliana (Reinhardt, 2005). For example, mutants in auxin transport, synthesis or perception fail to produce normal phyllotactic
arrangements and often develop leafless shoots (Bohn-Courseau,
2010; Besnard et al., 2011). These and other mutants indicate that
auxin plays an important role during the formation and positioning of new organs (Benková et al., 2003; Reinhardt et al., 2003;
Reinhardt, 2005). The lateral inhibition mechanism is consistent
with the observation that organ initiation sites are loci of high levels
of auxin activity (Benková et al., 2003; Reinhardt, 2005; BohnCourseau, 2010), the observation that organ removal or ablation
affects subsequent organ positioning (Reinhardt, 2005), and that
the loss of function mutation of the auxin transporter PIN1 results in
a shoot that produces leaves but (almost) no flowers (Reinhardt et
al., 2003). These and other data support the proposition that auxin
constitutes or contributes to the generation of patterns necessary
for organ arrangement in vascular plants and possibly also in other
plant lineages (Benková et al., 2003; Křeček et al., 2009; BohnCourseau, 2010; Zazímalová et al., 2010; Wabnik et al., 2011).
The role of polar auxin transport in the generation of phyllotactic
patterns is further supported by in silico experiments that reproduce
observed patterns based on the assumption that auxin maxima
initiate organ formation (e.g., Jönsson et al., 2005). However,
instead of requiring the diffusion of an inhibitor molecule, these
computer models indicate that phyllotaxis may be determined by
the formation of auxin peaks and valleys (Bohn-Courseau, 2010)
in a manner that is similar to the ”canalization” mechanism put
forward by Sachs some decades ago (Sachs, 1991). (Canalization sensu Sachs involves a self-sustained concentration of auxin
in particular sites, in contrast to canalization sensu Waddington
(1957), which refers to a developing organism’s ability to produce
the same phenotype despite variation in genotype or environment).
In addition to auxin, expansins have been suggested to act
as primordia initiators (Reinhardt et al., 1998; Fleming, 2006). As
discussed in the context of the POL DPM, there appears to be a
relation between the local mechanical properties of the wall and
the localization of auxin transporters. Indeed, it has been proposed
that the effects of physical forces acting on the cell wall might play
a key role in primordia formation and phyllotactic patterning (Newell
et al., 2008; Kierzkowski et al., 2012; for a review see Besnard
et al., 2011). For instance, it has been suggested that the rapid
growth of hypodermal cells in the shoot apical meristem exerts
forces on the tunica, such that when outer cell walls are loosened,
these compressive forces give rise to buckling patterns that closely
resemble the pattern of emerging primordia (Green et al., 1996;
Newell et al., 2008; Kierzkowski et al., 2012). In this scenario,
lateral inhibition between primordia is mediated or reinforced by
mechanical forces.
Liquid deformations, involving, e.g., viscous flow and surface
tension (Manning et al., 2010), are part of some of the proposed
animal DPMs (Newman and Bhat, 2008, 2009). The liquidity of
animal tissues, however, relies on the individual mobility of cells,
which is not observed in developing plant tissues. Instead, plastic
deformation, which in physics refers to the non-reversible changes
of a material in response to applied forces, seems to play an important role in plant growth.
Even though most plant tissues are viscoelastic solids, and
many are truly rigid solids (Niklas, 1992) the growth of plant cells
requires that cell walls become locally plastic, by means of cell
wall loosening, and deform under the force of turgor pressure, and
subsequently rigidify. Indeed, this deformation allows the cell to
increase its size permanently. Even if it is embedded in relatively
rigid tissue, or in rapidly growing tissues, the cell walls of groups of
cells can remain in phase, going through episodes of coordinating
softening and hardening. Expansins have been associated with
both elastic (i.e., reversible) and plastic (i.e., irreversible) changes
in the plant cell wall (Cosgrove, 2000). These effects reinforce auxin
patterns and thus contribute to the process by which different types
of mechanical forces contribute to the specification of new buds
(BUD DPM) (see Kierzkowski et al., 2012).
Expansins have been found or predicted to be present in several
lineages of embryophytes (Cosgrove, 2000; Carey and Cosgrove,
2007) and recent investigations suggest that these proteins are
also present in Micrasterias denticulata (Vannerum et al., 2011), a
green algae belonging to closest extant unicellular relatives of land
plants. This, along with the phyletic distribution patterns of auxin
and auxin transport (see discussion for POL DPM), suggest that
co-option of molecular mechanisms already present in unicellular
plants may have provided the basis for the BUD DPM.
Formation and shaping of leaf-like structures (LLS)
As first suggested by J. W. Goethe (1790), recent theoretical
studies based on experimental data (Pelaz et al., 2001) indicate
that floral organs and all other exogenously growing appendicular
structures can be classified as leaves. Therefore, it is reasonable to
speculate that another module in plant development may involve the
formation and shaping of leaf-like structures (LLS, Table 1; Fig. 3).
Leaf shape in particular is attained by anisotropic growth in several axes: the adaxial-abaxial, medial-lateral and proximal-distal.
The bulge formed by a feedback between biophysical and biochemical signals (BUD DPM) extends to create a functional leaf-like
structure and it has been hypothesized that in such growing organs,
the inner tissues are the driving forces for expansion, whereas the
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V. Hernández-Hernández et al.
outer tissues impose mechanical constraints and restrict the cell
expansion and organ growth (Fleming, 2006; Kutschera and Niklas,
2007). This proposal has been called epidermal-growth control;
just as the cell wall is a rigid structure that keeps the cell contents
under compression, restricts cell expansion and prevents the cell
from exploding, the epidermis and cuticle confines the expansion of
internal tissues during the growth of leaves and stems (Kutschera
and Niklas, 2007).
As described for the BUD DPM, the maturation of leaves may
involve interactions among the mechanical forces generated by
the epidermis and hypodermal cells. The balancing of these mechanical forces postulated to occur in leaf-like organs (Kutschera,
1989) may generate buckling phenomena that determine organ
curvatures and other aspects of leaf morphogenesis (Moulia,
2000; Dumais, 2007). Another component of the LLS DPM may
be the action of morphogens controlling the oriented growth and
tissue deformation during leaf growth, as suggested by a recent
study using time-lapse imaging, clonal analysis and computational
modeling (Kuchen et al., 2012).
Besides growth, leaf structure and physiology are influenced
by polarization patterns that establish the future distribution of cell
types (Moon and Hake, 2011). For example, cells in the adaxial
surface of the lamina are more important for light harvesting than
cells above the abaxial side, which play a more important role in
gas exchange. In this regard, Fleming (2006) has suggested that
changes in patterns of cell division respond to and induce mechanical signals that participate in subsequent developmental events
(see FCW DPM). The resulting new patterns of cell division may in
turn establish patterns of plasmodesmatal connections, ensuring
that ”groups of cells entering a particular developmental pathway
share relevant transcriptional information” in a way that they constitute ”separate entities” (Fleming, 2006). This could explain how
specific families of transcription factors are expressed by groups of
cells in the specification of leaf axes such as HD-ZIPIII family and
KANADI in the adaxial and abaxial sides, respectively (Braybrook
and Kuhlemeier, 2010; Moon and Hake, 2011). Another, nonexclusive explanation relies on the local production and apoplastic
transport of ligands or other types of signals that contribute to the
emergence of different expression profiles and the specification
of ”plasmodesmatal domains” within an organ.
Finally, leaf shape and vasculature differentiation are intimately
connected (Tsukaya, 2006). For example, auxin gradients generated by polar transport and canalization sensu Sachs (POL DPM)
determine the location of procambial cells that will subsequently
differentiate into the xylem and phloem (Sachs, 1991; Fujita and
Mochizuki, 2006) in ways that link the LLS and POL modules.
As is the case for other DPMs, the evolution of the LLS DPM
is also tightly associated with the evolution of the cell wall components, many of which could have been co-opted during the early
evolution of multicellular plants from pre-existing molecules and
processes. While, to the best of our knowledge, the information
required to situate the LLS module outside embryophtes (e.g., for
the laminar structures of bryophyte gametophytes) is still scarce,
this module offers a working hypothesis to continue studying this
process in other plant lineages.
Discussion
Fig. 4. The combination of the dynamical patterning modules (DPMs)
in different parts of an organism, and at different stages of development may give rise to the basic multicellular plant body plan. The
documented interactions among DPMs suggest that these modules may
act simultaneously or in an alternating manner along plant development,
therefore, this figure illustrate only one possible – although arguably common – sequence of DPM action and combination.
We have presented a preliminary set of dynamical patterning
modules (DPMs) associated with critical plant developmental
events (Table 1) and have specified some of the physical and molecular components of these modules. On the basis of the phyletic
distribution of the molecular elements of the DPMs, we have also
hypothesized that, as in animal systems, these modules originated
from co-option of cell-molecular mechanisms that had first evolved
in association with single-cell functions in the unicellular ancestors
of the various plant lineages which mobilized, in the multicellular
context, novel physical processes such as the internal mechanical
stresses generated as cells or tissues expand and grow. One of
our central conclusions is that not all of the information required for
plant development needs to be encoded genetically. Once development is set into operation, much of it becomes self-organizing.
Additionally, we suggest that the combination of different DPMs
at different places and developmental stages may be sufficient
for the generation of the basic features of the multicellular plant
body plan (Fig. 4).
We have assumed (as suggested by the ”module” nomenclature) that DPMs are semi-autonomous, which allows them to be
defined and studied separately. However, the proposed DPMs have
been shown to interact with one another, sometimes establishing
Dynamical patterning modules in plant evo-devo 671
negative and positive feedback systems. Indeed, it is the dynamic
combination and changing links among DPMs that could contribute
to the striking plasticity of plant development. For instance, it has
been observed that the relative positions of cell walls change with
cell growth and that the FCW module may also depend on cell
polarity (Dhonukshe et al., 2012).
DPMs provide a framework for comparing developmental
processes at a dynamic, epigenetic level, utilizing processes not
encoded directly in the DNA sequence. The methods to systematically perform such comparative analyses and infer evolutionary
relations are still relatively primitive. However, mathematical and
computational models will be extremely useful as tools to study
the collective action of a set of interacting molecules and physical processes constituting a DPM, as well as to test the behavior
of potential modifications of these modules with changes due to
mutation of DPM-enabling genes, or geometric context. For example, Zhu and coworkers (2010) have developed a model for the
system of DPMs associated with limb development in vertebrates
and have modeled modified versions that may correspond to the
alteration of relevant biological parameters, offering a mechanistic
explanation for the development and evolution of vertebrate limbs.
Additionally, DPMs serve as new evolutionary hypotheses that
are testable at many levels. The original DPM proposal suggests
that the combination of DPMs had an important role in the evolutionary origin of animal body plans and their early diversification
(Newman and Bhat, 2008, 2009). Specifically, this proposal suggests that early multicellular organisms were phenotypically plastic,
which permitted them to rapidly explore morphospace. In turn,
the relatively stable developmental trajectories and morphological phenotypes of modern organisms are a result of canalization
(e.g., via gene duplication and subspecialization) and stabilizing
selection. Indeed, it has been hypothesized that the collective
action of animal DPMs could have underlain the diversification of
bilaterian animal forms during the so-called Cambrian explosion
(Newman, 2012).
Here we speculate that, as suggested for animal systems, the
combined action of relatively flexible DPMs had a central role in
the evolution and diversification of plant body plans. This view
contrasts with the hypothesis that land plant diversification resulted
mainly from the expansion of particular gene families, such as PINs
(Zažímalová et al., 2010), or that the evolution of the embryophytes
was predominantly the result of hormonal dynamics (Cooke et al.,
2003). Certainly, while these molecules are central for plant development and, most probably also for plant morphological evolution,
we argue that the notion that diversification of certain gene families
or molecules classes can be the main cause of morphological
evolution is likely insufficient if not fundamentally flawed (Niklas
and Kutschera, 2012). In light of inconclusive searches for ”master”
molecules of animal embryogenesis (e.g., attempts to identify the
molecular basis of the vertebrate ”organizer”; Slack, 2002), we
believe that plant development is the result of a set of dynamical
systems that act synergistically in complex ways. In this picture,
gene products do not have fixed developmental roles over the
course of evolution, but take on new functions in different contexts.
More broadly, the DPM concept may help overcome the limitations of comparing and studying the evolution of genes or gene
families. For example, PINs do not seem to be expressed in moss
gametophytes. Nevertheless, the DPM formalism supports the investigation of cellular and organ polarity on the basis of interactions
between analogous ancient physiological and cell-wall properties
that do not rely on PINs.
As was the case in the evolution of animal development (Newman
and Bhat, 2009), generic physical effects were mobilized during the
early evolution of multicellular plants by particular gene products
and pathways. During this phase of evolution, some molecules
(an ”interaction toolkit” very different from that of the metazoans)
assumed critical importance in the development and continue to
do so among present-day plants. For example, auxin, which is
involved in regulating embryo and postembryonic development in
modern vascular plants, and is thus an important molecule in two
of the DPMs described here (Table 1), played a crucial role in the
diversification of land plant phenotypes during the Late Silurian to
Early Devonian Periods (Cooke et al., 2003; Niklas and Kutschera
2009, 2012). Additionally, our current knowledge of auxin action
and regulation suggests that major changes in auxin action occurred in the earliest land plants before the Late Silurian (Cooke et
al., 2003). However, the central role of auxin in plant development
and evolution cannot be understood without considering equally
ancient cell wall components, auxin transporters, etc. (Niklas and
Kutschera, 2012) as well as the physical processes collectively
mobilized by these molecules and their respective DPMs (Table 1).
Like auxin, cell wall components are involved in all of the proposed
DPMs, suggesting that the presence of a cell wall played a pivotal
role in determining and influencing the types of physical processes
that predominate during plant development. The mechanical forces
generated within and by plant cell walls stand in contrast to those
postulated for animal DPMs, which permit cell rearrangement and
deformations in a physical system that is largely defined by fluid
as opposed to solid mechanics (Newman and Bhat, 2008, 2009).
This difference suggests to us that the DPMs of multicellular fungi
might be more similar to those of plants than animals despite the
biochemical differences between the cell walls of fungi and plants
and the phylogenetic affinities of the fungi and the metazoans
(Shalcchian-Tabrizi et al., 2008).
Another difference between plant and animal DPMs concerns
the extent to which they are developmentally ‘flexible’ in evolutionarily more derived lineages. The original proposal concerning
animal DPMs postulated that these modules were initially flexible
in terms of phenotypic outcome but that they became integrated
into more robust and less plastic developmental processes, possibly via canalization (sensu Waddington) and selection. This may
have also been the case for plant development and evolution but
to a lesser degree for lineages in which sessile multicellular organisms evolved. In these lineages, it is reasonable to conjecture
that natural selection would have favored plants that retained
implementation of more plastic DPMs, particularly those with an
open indeterminate growth pattern in which new tissues or organs
are added indefinitely over the course of a life-time. Less rigidly
integrated systems of DPMs would permit development to track
changes in ambient environmental conditions, which can change
sometimes dramatically over the course of long-lived species
such as trees. This conjecture is amenable experimentally to falsification by means of broad developmental comparisons among
unicellular versus multicellular organisms and determinate versus
indeterminate species.
Finally, related to these questions of plasticity and flexibility
are insights into the mechanistic bases of these phenomena in
plants afforded by the DPM framework. In comparisons of animal
672
V. Hernández-Hernández et al.
and plant biology it has always been somewhat paradoxical that
multicellular plants, with their ”solid” tissue structure, are actually
more variable ecophenotypically and more capable of regenerating
lost parts, propagating vegetatively, morphologically accommodating grafts across species lines, and even forming new species by
hybridization, than their largely soft-tissued animal counterparts.
Considering plant development from the viewpoint of the DPMs
described above, it becomes clear that plant development, much
more so than animal embryogenesis, organizes matter that is dynamic over large scales, utilizing inherently multicellular systems
of multifunctional hormones/morphogens/transcription factors
which are unrestricted by cell boundaries in many of their functions. Under such conditions, the repurposing of adult tissues
for development, and the capacity to assume novel, ecologically
adaptive, morphological phenotypes within individual lifetimes,
becomes less enigmatic.
Acknowledgements
The authors would like to thank Elena R. Alvarez-Buylla, Alma PiñeyroNelson, Mario A. Pacheco, Ricardo Chávez, Eugenio Azpeitia, the members
of the De Folter (LANGEBIO) group, the members of the Theoretical Biology
Seminar at the Centro de Ciencias de la Complejidad C3, an anonymous
reviewer, as well as the participants in the Summer School on Evolutionary
Developmental Biology (Venice, 2011) for valuable discussions and comments regarding the ideas presented in this review. M.B. was supported
by the ‘‘CEITEC – Central European Institute of Technology’’ project
(CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund.
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